CASE REPORT Open Access

Hemorrhagic stroke in children caused byBothrops marajoensis envenoming: a casereportPedro Pereira de Oliveira Pardal1*, Augusto Cezar Jennings da Silva Pinheiro2, Cristiane Tarcis Cunha Silva2,Paulo Roberto Silva Garcez Santos2 and Maria Apolônia da Costa Gadelha1

Abstract

According to the World Health Organization, snakebites are considered neglected diseases. Bothrops, the genusmost frequently implicated in envenomations in Brazil, includes the species B. marajoensis Hoge, 1966, part of thecomplex B. atrox, which is found in the savannas of Marajó Island, Pará state, Brazil, a region that presents scarceepidemiological data. This work reports the first case of hemorrhagic stroke in a child, attributed to delayed medicalcare after snakebite envenoming by Bothrops marajoensis in Anajás city, Marajó Island, Pará, Brazil, which led topermanent hemiplegia as a sequela.

Keywords: Hemorrhagic stroke, Sequel, Bothrops marajoensis, Marajó Island

BackgroundSnakebites were included by the World HealthOrganization on the list of neglected diseases [1, 2]. An in-cidence of 5 million envenomings annually worldwide isestimated, with the highest incidence in developing coun-tries with agricultural activities [3]. In Latin America thereare approximately 129,084 cases annually, with the vastmajority being caused by species of the family Viperidae[4]. In Brazil, from 2011 to 2014 there were 112,249 acci-dents, 72 % caused by Bothrops [5].The genus Bothrops has neotropical distribution,

with the species B. marajoensis Hoge, 1966 [6] beingfound in the savannas of Marajó Island, Pará state,Brazil [7]. This species is part of the complex B.atrox, popularly known as “jararaca”, “surucucurana”,“combóia” and even by “surucucu” [8]. The Bothropsare implicated in a large number of envenomings inthe Brazilian Amazon, where they affect mainly ruralareas and are considered a public health problem. Theepidemiological data on this species are scarce and under-estimated in this region [9, 10].

Snake venom is a complex mixture containing bio-logically active peptides and proteins that can cause localinflammatory responses and changes of blood coagulationdue to defibrination, disseminated intravascular coagulationand thrombocytopenia resulting in partial or completeblood incoagulability, leading to systemic bleeding that mayprovoke a hemorrhagic stroke [11–13]. But in children thispicture is poorly described, which encouraged us to reportthe first case associated with snakebite envenomingby B. marajoensis [14, 15].

Case presentationA male child younger than 10 years old, from Anajáscity, Marajó Island, Pará (latitude 00°59'14" and longi-tude 49°56'25") (Fig. 1), was bitten in an attack by asnake identified as B. marajoensis Hoge, 1966 [6] (Fig. 2),in the plantar region of the right foot, on July 14, 2013,while harvesting açaí.After the bite, the patient reported local pain then

local edema. His parent took him by motorized boat formedical assistance in Anajás. During the trip the boatmalfunctioned, which delayed medical care for 25 h.During transport, the child became somnolent andstopped communicating. Upon admission at the hospital,he presented with edema on the entire right leg,

* Correspondence: pepardal@ufpa.br1University Hospital João de Barros Barreto, Federal University of Pará (UFPA),Rua dos Mundurucus 4487, Guamá, 66073.000, Belém, PA, BrasilFull list of author information is available at the end of the article

© 2015 de Oliveira Pardal et al. Open Access This article is distributed under the terms of the Creative Commons Attribution4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

de Oliveira Pardal et al. Journal of Venomous Animals andToxins including Tropical Diseases (2015) 21:53 DOI 10.1186/s40409-015-0052-5

http://crossmark.crossref.org/dialog/?doi=10.1186/s40409-015-0052-5&domain=pdfmailto:pepardal@ufpa.brhttp://creativecommons.org/licenses/by/4.0/http://creativecommons.org/publicdomain/zero/1.0/

ecchymosis, blisters, hematuria and a comatose state,and was classified as severely poisoned.The child received all four vials of antibothropic anti-

venom available in the service unit. A transfer to Belémcity, the capital of Pará state, was requested, andeffected 2 days after to the Emergency DepartmentMario Pinotti by helicopter. He was admitted with the

aforementioned clinical manifestations and the sameseverity, with eight antivenom vialshaving been infusedto complete the number of ampoules required due tothe gravity of the case.He was transferred on 19 July to the University Hospital

João de Barros Barreto in Belém, where he was admitted co-matose, with right hemiplegia, labial commissure deviation

Fig. 1 Map of Marajó Island in the state of Pará, highlighting the city of Anajás, the envenomation site

de Oliveira Pardal et al. Journal of Venomous Animals and Toxins including Tropical Diseases (2015) 21:53 Page 2 of 5

to the left side (Fig. 3), heart and lung auscultation withoutabnormalities, swelling from the foot to the knee, blisters,normal urinary color and volume and signs of infection atthe bite site.He was evaluated by a neurologist who requested la-

boratory tests (Table 1) and acomputed tomography ofthe brain that showed hemorrhagic lesions (Fig. 4). Con-servative therapeutics and antibiotic therapy were ap-plied. During the 19 days of hospitalization, the patientreceived medical and physiotherapist follow-up, receiv-ing medical discharge with sequelae including right flac-cid hemiplegia.

DiscussionA case of hemorrhagic stroke in a child associated withenvenoming by B. marajoensis in Anajás city, MarajóIsland, is herein reported. This type of accident in thepediatric age group is rarely described in the literature,

but is more frequently reported in adults. Mosquera,Idrovo and Tafur [16] reported an incidence of 2.6 % ofstrokes in Bothrops victims in Ecuador, where as Thomaset al. [17] found 2.3 % in Martinique. Santos-Soares etal. [18] and Machado et al. [19] also reported cases ofstroke following snakebites in Brazil.Bothropsis the main genus involved in snakebites in

Brazil [20]. In the Amazon, ophidic accidents are attrib-uted mostly to B. atrox species complex, represented inthe archipelago of Marajó by B. marajoensis [21, 22]. Inall 144 cities of Pará state in the 2012–2014 period, there

Fig. 3 Labial commissure deviation to the left side

Table 1 Laboratory tests conducted at the Hospital João deBarros Barreto on July 19, 2013

Exams Results Reference values

Hemogram 3.61 millions/mm3 4.4 to 5.9 millions/mm3

Hemoglobin 10.3 g/dL 13.8 to 18.0 g/dL

Hematocrit 31.1 % 40 to 52 %

Leukogram 6.54/mm3 5,000 to 10,000/mm3

Segmented 90 % 40 to 75 %

Platelet count 121,000/mm3 130,000 to 400,000/mm3

APTTa 20.3 s 25 to 34 s

Urea 27 mg/dL 10 to 40 mg/dL

Creatinine 0.5 mg/dL 0.4 to 1.2 mg/dL

Creatine kinase (CK) 915 lU/mL fem

were 14,842 snakebite accidents in total; of these,86.84 % by Bothrops. Two thousand two hundred andseventy-one (2271, i.e., 15.3 %) of these envenomings oc-curred in the 16 cities of Marajó Island [5].The venom of snakes of the genus Bothrops are complex

mixtures of proteins and peptides that present varioustoxic activities leading to inflammatory, coagulant andhemorrhagic effects [12, 23]. Symptoms of envenoming aredetermined by the type of venom, the agent, the severity ofthe accident and by the conditions inherent to the victim,which may include local manifestations (pain, swelling andredness) and systemic manifestations (bleeding). Complica-tions of envenoming with hemorrhagic stroke are more evi-dent in patients with preexisting risk factors such ascardiovascular disease, particularly systemic hypertension,which was not detected in this case [19, 24].The accident occurred in the country side, when the

child was descending an açaí palm tree (Euterpe oleracea),which bears a berry much appreciated by people and is avery popular food supplement. Snakebite is a commonand frequently devastating occupational and environmen-tal disease, especially in rural areas of tropical developingcountries [25].The accident site is about 7 hours away from medical

care. Using a motorboat, however, the patient was onlyable to reach the hospital of the municipal headquarters25 h after the event, due to engine failure on the boatthat was transporting him. This is a common situationin the region, as the medical care is distant from whereaccidents normally occur. The precarious means oftransport greatly aggravates the clinical condition of thevictims. It is recommended by the Brazilian Ministry ofHealth that the initial care of the patient bitten by ven-omous animals should be obtained as soon as possible,with the number of vials based on the severity of the ac-cident [20]. In this case, the initial treatment should con-sisted of 12 ampoules of antivenom. In Brazil, theantivenom used is liquid and requires electricity for itsconservation, which delays treatment, since accidentsoccur in rural areas [20]; hence, if we had lyophilizedserum in these regions, we believe that similar caseswould not occur.Hemorrhagic stroke is characterized by bleeding into

brain tissue, the cerebellum, or brain stem, usually byrupture of a small vessel, causing the overflowed bloodunder pressure in the brain tissue to lead to clinicalmanifestations that depend on the location and the spe-cific extent of bleeding [26]. The signs and symptomsobserved in the present case included an acute onsetwithout history of trauma and progressed to drowsinessand coma. In the United States, half of pediatric strokesare caused by bleeding in association with several othercauses, but without references to envenoming by snakes[27]. In Brazil, Bucaretchi et al. [28] did not find any

cases of stroke in 322 children envenomed by snakes. Inour case, the clinical examination revealed right hemiplegiaand deviation of the labial commissure to the left, while thecranial computed tomography scan showed bleeding lesionin the right frontal area, which characterized an acuteneurological presentation of hemorrhagic stroke [16].Intracerebral hemorrhage after snakebite is related to

the occurrence of severe coagulopathy, which is notshown in this case due to the fact that the tests had beenadministered belatedly [29]. Pardal et al. [9] showed thatB. atrox was responsible for 13.3 % of blood incoagulabil-ity while Ribeiro et al. [30] reported four cases of intrace-rebral hemorrhage caused by Bothrops that presentedcoagulopathy. These brain bleeding disorders have beenlinked with incoagulability and low platelet count associ-ated with brain capillary endothelial damage caused byhemorrhages and possibly by other toxins found in thesnake venom [12, 31]. Other laboratory exams such asblood count showed anemia, while total creatine phospho-kinase appeared five times higher than the reference value,which is related to the inflammatory process at the bitesite and brain injury in this case. This enzyme is mainlyused to assess changes in the heart muscle, skeletal muscleand brain [31].

ConclusionThis is the first case report of hemorrhagic stroke in achild attributed to delayed medical care after snakebiteenvenoming by Bothrops marajoensis on the island ofMarajó, which led to permanent hemiplegia as a sequela.

ConsentWritten informed consent was obtained from the legalguardian of the patient for publication of this case reportand accompanying images.

Ethics committee approvalThis manuscript was approved by the Research EthicsCommittee of the University Hospital João de BarrosBarreto, document number 41157015.3.0000.0017.

Competing interestsThe authors declare that there are no competing interests.

Authors’ contributionsAll the authors observed the reported case and contributed to the design ofthe study and revision of the manuscript. All authors read and approved thefinal manuscript.

AcknowledgmentsWe thank the physicians and physiotherapists from the University HospitalJoão de Barros Barreto for their collaboration in patient care and LeandroOliveira for photography of B. marajoensis.

Author details1University Hospital João de Barros Barreto, Federal University of Pará (UFPA),Rua dos Mundurucus 4487, Guamá, 66073.000, Belém, PA, Brasil. 2School ofMedicine, Federal University of Pará (UFPA), Belém, PA, Brazil.

de Oliveira Pardal et al. Journal of Venomous Animals and Toxins including Tropical Diseases (2015) 21:53 Page 4 of 5

Received: 23 June 2015 Accepted: 21 November 2015

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http://www.who.int/neglected_diseases/integrated_media_snakebite/en/http://dtr2004.saude.gov.br/sinanweb/tabnet/dh?sinannet/animaisp/bases/animaisbrnet.defhttp://dtr2004.saude.gov.br/sinanweb/tabnet/dh?sinannet/animaisp/bases/animaisbrnet.defhttp://dtr2004.saude.gov.br/sinanweb/tabnet/dh?sinannet/animaisp/bases/animaisbrnet.defhttp://repositorio.unb.br/bitstream/10482/11108/1/2012_JessicaFenkerAntunes.pdfhttp://repositorio.unb.br/bitstream/10482/11108/1/2012_JessicaFenkerAntunes.pdf

AbstractBackgroundCase presentationDiscussionConclusionConsentEthics committee approvalCompeting interestsAuthors’ contributionsAcknowledgmentsAuthor detailsReferences